Identification of the molecular mechanisms by which the diterpenoid salvinorin A binds to κ-opioid receptors

Biochemistry

Volumn 44, Issue 24, 2005, Pages 8643-8651

  Yan, Feng ^a   Mosier, Philip D ^b   Westkaemper, Richard B ^b   Stewart, Jeremy ^c   Zjawiony, Jordan K ^c   Vortherms, Timothy A ^a   Sheffler, Douglas J ^a   Roth, Bryan L ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c UNIVERSITY OF MISSISSIPPI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIPIDS; MOLECULAR DYNAMICS; MOLECULES; MUTAGENESIS; POLYPEPTIDES; PROTEINS;

BINDING AFFINITY; G-PROTEIN COUPLED RECEPTOR (GPCR); SALVINORIN A; TYROSINE;

PLANTS (BOTANY);

2 THIOSALVINORIN B; CYSTEINE; DITERPENOID; DYNORPHIN[1-13]; G PROTEIN COUPLED RECEPTOR; KAPPA OPIATE RECEPTOR; KAPPA OPIATE RECEPTOR AGONIST; N METHYL N [7 (1 PYRROLIDINYL) 1 OXASPIRO[4.5]DEC 8 YL]BENZENEACETAMIDE; PSYCHEDELIC AGENT; SALVINORIN A; THIOL GROUP; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; DRUG RECEPTOR BINDING; DRUG SELECTIVITY; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RECEPTOR AFFINITY; SALVIA; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; BINDING SITES; DITERPENES; DNA, COMPLEMENTARY; HUMANS; KINETICS; MODELS, MOLECULAR; PROTEIN STRUCTURE, SECONDARY; RECEPTORS, OPIOID, KAPPA; RECOMBINANT PROTEINS; SALVIA;

SALVIA DIVINORUM;

EID: 20544441511     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi050490d     Document Type: Article

References (34)

1. Valdes, L. J., Butler, W. M., Hatfield, G. M., Paul, A. G., and Koreeda, M (1984) Divinorin A: A psychotropic terpenoid and divnorin B from the hallucinogenic Mexican mint Salvia divinorum. J. Org. Chem. 49, 4716-7720.
2. Valdes, L. J., III, Diaz, J. L., and Paul, A. G. (1983) Ethnopharmacology of ska Maria Pastora (Salvia divinorum, Epling and Jativa-M.). J. Ethnopharmacol. 7, 287-312.
3. Siebert, D. J. (1994) Salvia divinorum and salvinorin A: New pharmacologic finding, J. Ethnopharmacol. 43, 53-56.
4. Roth, B. L., Baner, K., Westkaemper, R., Siebert, D., Rice, K. C., Steinberg, S., Ernsberger, P., and Rothman, R. B. (2002) Salvinorin A: A potent naturally occurring nonnitrogenous κ opioid selective agonist, Proc. Natl. Acad. Sci. U.S.A. 99, 11934-11939.
5. Sheffler, D. J., and Roth, B. L. (2003) Salvinorin A: The "magic mint" hallucinogen finds a molecular target in the κ opioid receptor, Trends Pharmacol. Sci. 24, 107-109.
6. Chavkin, C., Sud, S., Jin, W., Steward, J., Zjawiony, J. K., Siebert, D., Toth, B. A., Hufeisen, S. J., and Roth, B. L. (2004) Salvinorin A, an active component of the hallucinogenic sage Salvia divinorum, is a highly efficacious κ opioid receptor agonist: Structural and functional considerations, J. Pharmacol. Exp. Ther. 308.
7. Wang, Y., Tang, K., Inan, S., Siebert, D. J., Holzgrabe, U., Lee, D. Y., Huang, P., Li, J. G., Cowan, A., and Liu-Chen, L. Y. (2004) Comparison of pharmacological activities of three distinct κ ligands (salvinorin A, TRK-820, and 3FLB) on κ opioid receptors in vitro and their antipruritic and antinociceptive activities in vivo, J. Pharmacol. Exp. Ther. 308.
8. Ballesteros, J. A., Shi, L., and Javitch, J. A. (2001) Structural mimicry in G protein-coupled receptors: Implications of the high-resolution structure of rhodopsin for structure-function analysis of rhodopsin-like receptors, Mol. Pharmacol. 60, 1-19.
9. Shapiro, D. A., Kristiansen, K., Weiner, D. M., Kroeze, W. K., and Roth, B. L. (2002) Evidence for a model of agonist-induced activation of 5-HT2A serotonin receptors which involves the disruption of a strong ionic interaction between helices 3 and 6, J. Biol. Chem. 18, 18.
10. Shi, L., and Javitch, J. A. (2004) The second extracellular loop of the dopamine D2 receptor lines the binding-site crevice, Proc. Natl. Acad. Sci. U.S.A. 101, 440-445.
11. Shapiro, D. A., Kristiansen, K., Kroeze, W. K., and Roth, B. L. (2000) Differential modes of agonist binding to 5-hydroxytryptamine-(2A) serotonin receptors revealed by mutation and molecular modeling of conserved residues in transmembrane region 5, Mol. Pharmacol. 58, 877-886.
12. Kristiansen, K. (2004) Molecular mechanisms of ligand binding, signaling, and regulation within the superfamily of G-protein-coupled receptors: Molecular modeling and mutagenesis approaches to receptor structure and function, Pharmacol. Ther. 103, 21-80.
13. Stewart, D. J. Doctoral Dissertation, University of Mississippi, February 25, 2005.
14. Chavkin, C., Sud, S., Jin, W., Stewart, J., Zjawiony, J. K., Siebert, D. J., Toth, B. A., Hufeisen, S. J., and Roth, B. L. (2004) Salvinorin A, an active component of the hallucinogenic sage Salvia divinorum is a highly efficacious κ-opioid receptor agonist: Structural and functional considerations, J. Pharmacol. Exp. Ther. 308, 1197-1203.
15. Westkaemper, R. B., and Glennon, R. A. (2002) Application of ligand SAR, receptor modeling, and receptor mutagenesis to the discovery and development of a new class of 5-HT(2A) ligands, Curr. Top. Med. Chem. 2, 575-598.
16. Baldwin, J. M., Schertler, G. F., and Unger, V. M. (1997) An α-carbon template for the transmembrane helices in the rhodopsin family of G-protein-coupled receptors, J. Mol. Biol. 272, 144-164.
17. Palczewski, K., Kumasaka, T., Hori, T., Behnke, C. A., Motoshima, H., Fox, B. A., Le Trong, I., Teller, D. C., Okada, T., Stenkamp, R. E., Yamamoto, M., and Miyano, M (2000) Crystal structure of rhodopsin: A G protein-coupled receptor [see comments], Science 289, 739-745.
18. Bower, M. J., Cohen, F. E., and Dunbrack, R. L., Jr. (1997) Prediction of protein side-chain rotamers from a backbone-dependent rotamer library: A new homology modeling tool, J. Mol. Biol. 267, 1268-1282.
19. Ronsisvalle, G., Pasquinucci, L., Pappalardo, M. S., Vittorio, F., Fronza, G., Romagnoli, C., Pistacchio, E., Spampinato, S., and Ferri, S. (1993) Non-peptide ligands for opioid receptors. Design of κ-specific agonists, J. Med. Chem. 36, 1860-1865.
20. Lavecchia, A., Greco, G., Novellino, E., Vittorio, F., and Ronsisvalle, G. (2000) Modeling of κ-opioid receptor/agonists interactions usins pharmacophore-based and dockine simulations, J. Med. Chem. 43, 2124-2134.
21. Mansour, A., Taylor, L. P., Fine, J. L., Thompson, R. C., Hoversten, M. T., Mosberg, H. I., Watson, S. J., and Akil, H. (1997) Key residues defining the μ-opioid receptor binding pocket: A site-directed mutagenesis study, J. Neurochem. 68, 344-353.
22. Sharma, S. K., Jones, R. M., Metzger, T. G., Ferguson, D. M., and Portoghese, P. S. (2001) Transformation of κ-opioid receptor antagonist to a κ-agonist by transfer of a guanidinium group from the 5′- to 6′-opposition of naltrindole, J. Med. Chem. 44, 2073-2079.
23. Larson, D. L., Jones, R. M., Hjorth, S. A., Schwartz, T. W., and Portoghese, P. S. (2000) Binding of norbinaltorphimine (norBNI) congeners to wild-type and mutant μ and κ opioid receptors: Molecular recognition loci for the pharmacophore and address components of κ antagonists, J. Med. Chem. 43, 1573-1576.
24. Meng, F., Hoversten, M. T., Thompson, R. C., Taylor, L., Watson, S. J., and Akil, H. .(1995) A chimeric study of the molecular basis of affinity and selectivity of the κ and the δ opioid receptors. Potential role of extracellular domains, J. Biol. Chem. 270, 12730-12736.
25. Watson, B., Meng, F., and Akil, H. (1996) A chimeric analysis of the opioid receptor domains critical for the binding selectivity of μ opioid ligands, Neurobiol. Dis. 3, 87-96.
26. Jones, G., and Willett, P (1995) Docking small-molecule ligands into active sites, Curr. Opin. Biotechnol. 6, 652-656.
27. Jones, G., Willett, P., Glen, R. C., Leach, A. R., and Taylor, R. (1997) Development and validation of a genetic algorithm for flexible docking, J. Mol. Biol. 267, 727-748.
28. Kong, H. Y., Raynor, K., and Reisine, T. (1994) Amino acids in the cloned κ receptor that are necessary for the high affinity agonist binding but not antagonist binding, Regul. Pept. 54, 155-156.
29. Ott, D., Frischknecht, R., and Pluckthun, A. (2004) Construction and characterization of a κ opioid receptor devoid of all free cysteines, Protein Eng. Des. Sel. 17, 37-48.
30. Xu, W., Li, J., Chen, C., Huang, P., Weinstein, H., Javitch, J. A., Shi, L., de Riel, J. K., and Liu-Chen, L. Y. (2001) Comparison of the amino acid residues in the sixth transmembrane domains accessible in the binding-site crevices of μ, δ, and κ opioid receptors, Biochemistry 40, 8018-8029.
31. Bourne, H. R., and Meng, E. C. (2000) Structure. Rhodopsin sees the light, Science 289, 733-734.
32. Fowler, C. B., Pogozheva, I. D., LeVine, H., III, and Mosberg, H. I. (2004) Refinement of a homology model of the μ-opioid receptor using distance constraints from intrinsic and engineered zinc-binding sites, Biochemistry 43, 8700-8710.
33. Pogozheva, I. D., Lomize, A. L., and Mosberg, H. I. (1998) Opioid receptor three-dimensional structures from distance geometry calculations with hydrogen bonding constraints, Biophys. J. 75, 612-634.
34. Kabsch, W., and Sander, C. (1983) Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features, Biopolymers 22, 2577-2637.